Invasion Biology of Ponto-Caspian Onychopod Cladocerans (Crustacea: Cladocera: Onychopoda)

Hydrobiologia (2007) 590:3–14 DOI 10.1007/s10750-007-0752-0

INVASIVE CRUSTACEA

Invasion biology of Ponto-Caspian onychopod cladocerans (Crustacea: Cladocera: Onychopoda)

Vadim E. Panov Æ Natalie V. Rodionova Æ Pavel V. Bolshagin Æ Eugene A. Bychek

Ó Springer Science+Business Media B.V. 2007

Abstract We review the patterns of recent range possess adaptive life cycles, switching to early expansions and the biology of the invasive Ponto- gamogenetic reproduction which enables their Caspian predatory onychopod cladocerans: establishment in recipient ecosystems and further Cercopagis pengoi, Evadne anonyx, Podonevadne dispersal. Analysis of temperature and salinity trigona, Cornigerius maeoticus and Cornigerius ranges of the Ponto-Caspian onychopod species bicornis. Recent invasions of C. pengoi, E. anonyx in native and invaded habitats, indicates that they and C. maeoticus into the Baltic Sea can be are potentially able to form populations in a wide attributed to the climate change, facilitating range of inland and coastal water ecosystems in invasibility of the eastern Baltic Sea coastal temperate zones. Ponto-Caspian onychopods can ecosystems by the warm water Ponto-Caspian be considered as ‘‘high risk’’ invasive species, in species and intensive shipping activities via the terms of their potential for range expansion and Volga-Baltic waterway (European ‘‘northern impact on recipient ecosystems. invasion corridor’’). All three species can be considered to be established in pelagic communi- Keywords Invasive crustaceans Á Onychopoda Á ties of the eastern Gulf of Finland. Only one Ponto-Caspian species Á Invasion history Á onychopod species, C. pengoi has invaded the Risk assessment North American Great Lakes via an existing invasion corridor between the eastern Baltic and the Great Lakes. Invasive onychopods may Introduction

The Ponto-Caspian region (the Black, Azov seas Guest editors: Elizabeth J. Cook and Paul F. Clark Invasive Crustacea and the Caspian Lake, including their basins) is serving as an important donor for invasive aquatic V. E. Panov (&) Á N. V. Rodionova Á alien species worldwide, speciﬁcally for European P. V. Bolshagin and North American inland waters, with shipping- Zoological Institute of the Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg related activities as a main vector of both inter- and 199034, Russia intracontinental dispersal (Mordukhai-Boltovskoi, e-mail: [email protected] 1964a; Panov et al., 1999; Ricciardi & MacIsaac, 2000; Reid & Orlova, 2002; Vanderploeg et al., E. A. Bychek Institute of Ecology of the Volga River Basin, RAS, 2002; Ketelaars, 2004; Galil et al., 2007). Within Togliatti 445003, Russia Europe, inland and coastal waters in the Baltic Sea

123 4 Hydrobiologia (2007) 590:3–14 and North Sea basins are the main recipient areas euryhalinity due to their evolution and, conse- for invasions of Ponto-Caspian species (Jazdzewski, quently, they are well adapted to invade new 1980; Bij de Vaate et al., 2002; Jazdzewski & environments, specifically C. pengoi, P. trigona and Konopacka, 2002; Ketelaars, 2004; Galil et al., C. maeoticus, which were found spreading outside 2007). At present, 22 fish and aquatic invertebrate their native range already in the mid 20th century species of Ponto-Caspian origin are successfully following the construction of reservoirs in the established in the Baltic Sea basin, comprising Dniepr, Don and Volga rivers (Mordukhai-Boltov- almost a third of all established non-indigenous skoi, 1979; Dumont, 2000). Moreover, Dumont aquatic species in the Baltic (Olenin et al., 2006). (2000) considered the origin of all known onycho- In the Laurentian Great Lakes during the last two pod species monophyletic; all 33 onychopod species decades, 8 Ponto-Caspian species have successfully were found to have originated in the Ponto-Caspian established themselves, causing significant ecolog- basin, with two freshwater and seven marine species ical impacts (Vanderploeg et al., 2002; Grigorovich possessing either a world-wide, or wide distribution et al., 2003a). Invasion success of Ponto-Caspian in the northern hemisphere as a result of natural species in inland and coastal waters outside their range expansion from the Ponto-Caspian area. native range can be attributed primarily to the Genetic studies of onychopods have revealed that euryhalinity of the Ponto-Caspian biota (Morduk- diversification of this group has occurred over the hai-Boltovskoi, 1964b; Dumont, 1998, 2000). past 10–20 million years and that disruptive selec- Intensive shipping activities in the Ponto-Cas- tion by predators is considered as the main driving pian region itself have also resulted in a number force in shaping the body plane diversity of onycho- of biological invasions in the Black, Azov seas pods (Cristescu & Hebert, 2002). and the Caspian, with severe economic and This group of obviously invasive species, how- ecological consequences for their ecosystems ever, has attracted serious attention of invasion (Shiganova et al., 2001; Grigorovich et al., 2002; biologists comparatively recently, after human- Grigorovich et al., 2003b; Dumont et al., 2004). mediated spread of the ‘‘freshwater Palearctic’’ As a consequence, the Ponto-Caspian region may Bythotrephes longimanus Leydig 1860 from east- serve as a secondary donor for these invasive ern Europe to North America and the ‘‘euryha- species via existing corridors, specifically to the line Ponto-Caspian’’ C. pengoi to the Baltic Sea Baltic and North seas. and North American Great Lakes (see reviews by Dispersal patterns of Ponto-Caspian species had Krylov et al., 2004 and Panov et al., 2004). been recently reviewed by Bij de Vaate et al. (2002) In the present paper, we have summarized and Ketelaars (2004). These reviews have further available information on invasion histories and developed the concept of inland European water- biology of Ponto-Caspian onychopods, which have ways as intracontinental invasion corridors from the expanded their native ranges in geographic Eur- Ponto-Caspian region to inland and coastal waters ope comparatively recently as a result of human- in the Baltic and North sea basins, an idea which was mediated invasions. This background information initially suggested for the Volga-Baltic inland water- is essential for developing approaches to risk way (Panov et al., 1999). These reviews, however, assessment of further spread and determining the have focused on benthic macroinvertebrate organ- ecological impacts of these invasive species. isms and comparatively low attention has been given to the invasive planktonic Ponto-Caspian predatory ‘‘cladocerans’’ (Crustacea: Branchiopoda: Onycho- Invasion history of Ponto-Caspian onychopods poda), which include 5 onychopod species found in the Black, Azov seas and the Caspian Lake, namely Cercopagis pengoi Cercopagis pengoi (Ostroumov, 1891), Evadne anonyx Sars, 1897, Podonevadne trigona (Sars, Cercopagis pengoi (Ostroumov, 1891) (Superor- 1897), Cornigerius maeoticus (Pengo, 1879) and der Cladocera: order Onychopoda: family Cerco- Cornigerius bicornis (Zernov, 1901) (Mordukhai- pagidae) is native to the Sea of Azov, Caspian Boltovskoi, 1964b; 1979). These species possess and Aral lakes (C. pengoi disappeared from the

123 Hydrobiologia (2007) 590:3–14 5 latter after an increase in salinity of the lake along et al., 2002; Krylov et al., 2004) (Fig. 1). In the with most other onychopods—see Rivier (1998)), Gulf of Finland, in areas of mass development of certain river estuaries of the Black Sea (Danube, C. pengoi (hundreds and thousands of ind. m3), Dnieper and Bug rivers) and the Gebenjinskoe fishing nets are often clogged by this species Lake in Bulgaria (Rivier, 1998). Between 1960– which results in severe economic losses for the 1975, after construction of the dams on the local coastal fishery (Panov et al., 1999). Don and Dnieper rivers in the Black Sea basin, In summer 1998, C. pengoi was found outside C. pengoi invaded the freshwater reservoirs of Eurasia for the first time, where it was recorded Kakhovka, Zaporozhsk, Kremenchug, Tsyml- snagged on sport fishing lines and in zooplankton yansk and Veselovsk (Krylov et al., 1999). Most samples in Lake Ontario in North America recently, in 2000–2005, C. pengoi was recorded (MacIsaac et al., 1999; Barbiero & Tuchman, in zooplankton samples from the Volga River 2000). Most likely, this is a result of secondary reservoirs; Volgograd, Saratov and Kuibyshev introduction by ships ballast water from the (Eugene A. Bychek unpubl.) (Fig. 1). eastern Baltic via an existing invasion corridor, In 1992, C. pengoi was first found outside the identified in case of Bythotrephes longimanus Ponto-Caspian basin in the Baltic Sea area (Gulf invasion by Berg et al. (2002). A recent genetic of Riga and Gulf of Finland), possibly as a result study by Cristescu et al. (2001) demonstrated that of the discharge of ballast water (Ojaveer & the population of C. pengoi in the North Amer- Lumberg, 1995; Ojaveer et al., 2000). After these ican Great Lakes is most likely to have originated first records, C. pengoi was found in the Neva from the Baltic Sea source population, namely the River estuary in 1995, already at high densities Neva Estuary (eastern Gulf of Finland). From and has since become a common zooplankton Lake Ontario, C. pengoi has spread in only a few species in the eastern Gulf of Finland (Panov, years to Lake Michigan, western Lake Erie and 1996; Avinsky, 1997; Krylov et al., 1999; Panov some adjacent inland lakes (Charlebois et al., et al., 1999; Uitto et al., 1999). In 1997, C. pengoi 2001; Therriault et al., 2002). was reported from the central Baltic Sea and Swedish coastal waters (Gorokhova et al., 2000) Cornigerius maeoticus and Cornigerius and in 1999, it had spread to the Gulf of Bothnia, bicornis Gulf of Gdansk and the lagoons of the southern Baltic Sea (Bielecka et al., 2000; Leppa¨koski Cornigerius maeoticus (Pengo, 1879) (Superorder Cladocera: order Onychopoda: family Podoni- dae) is native to the Sea of Azov, lower reaches of the Danube, Dniepr and Bug rivers and the Caspian Lake (Rivier, 1998). Rivier (1998) has also found by studying valve morphology in C. maeoticus, that there are two subspecies, C. maeoticus maeoticus (Pengo, 1879), inhabiting the Ponto-Azov area and C. maeoticus hircus (Sars, 1902), which is characteristic for the Cas- pian Lake. However, genetic evidence for the separation of Ponto-Caspian onychopods by subspecies is lacking (Cristescu & Hebert, 2002) and in present paper we have not considered the subspecies of C. maeoticus (see also case study of Podonevadne trigona). As in the case of Cercopagis pengoi, the Fig. 1 Distribution of Cercopagis pengoi in the native expansion of C. maeoticus (subspecies C. m. range (open cycles) and sites of first records of its range expansion (filled cycles). Dashed line indicate the ‘‘north- maeoticus sensu Rivier (1998)) outside its native ern invasion corridor’’ range, started after the creation of the reservoirs

123 6 Hydrobiologia (2007) 590:3–14 on the Don, Dnieper, and Volga rivers, with phology two subspecies of P. trigona, with C. maeoticus appearing in the Kakhovka (1959), subspecies P. trigona trigona (Sars, 1897) found Tsimlyansk (1961), Zaporozhsk (1965) and in the Caspian Lake. The other subspecies, Kremenchug (1969) reservoirs (Rodionova et al., P. trigona ovum (Zernov, 1901) is characteristic 2005). In the 1970s, this species was first recorded for the Ponto-Azov basin and after construction in the Volga River basin (Volgograd Reservoir) of reservoirs in the Dniepr and Don rivers, and in the remaining Dnieper River reservoirs it invaded Kahovka (1959), further reservoirs of (the Kiev, Kanev, Dneprodzerzhinsk and Ka- the Dniepr River and Don river basin and the khovka). In the mid 1990s, it was found in the Tsymlansk reservoir (1966) (Rivier, 1998) Saratov and Kuibyshev reservoirs of the Volga (Fig. 3). River (Eugene A.Bychek unpubl.). In 2003, C. maeoticus was first recorded outside the Ponto- Evadne anonyx Caspian basin in the eastern Baltic Sea (Rodio- nova et al., 2005) (Fig. 2). Evadne anonyx Sars, 1897 (Superorder Clado- The congeneric species with a known invasion cera: order Onychopoda: family Podonidae) is history, C. bicornis (Zernov, 1901) is mainly native to the Caspian and Aral lakes (currently it found in spring in the Sea of Azov and Caspian is not present in the Aral due to increased Lake and has expanded its native distribution salinity) and possibly the Ponto-Azov basin range to Tsymlyansk Reservoir and the Dniepr (Mordukhai-Boltovskoi, 1966; Rivier, 1998). Un- canals (Rivier, 1998). like other invasive onychopods, E. anonyx has no recent invasion history in the Ponto-Caspian Podonevadne trigona basin. However, in 2000 it was first recorded outside its native range in the eastern Gulf of Podonevadne trigona (Sars, 1897) (Superorder Finland, Baltic Sea and currently, this species can Cladocera: order Onychopoda: family Podoni- be considered to be well established in the dae) is native to the Caspian Lake, Sea of Azov easternmost Baltic (Rodionova & Panov, 2006) and the lagoons of the Dniestr, Dniepr and Bug (Fig. 4). This case study can be considered as an rivers (Rivier, 1998). As for Cornigerius maeoti- example of long-distance intracontinental transfer cus, Rivier (1998) distinguishes by valve mor- of alien species by ballast water directly from the Caspian Lake to the eastern Baltic Sea. Genetic

Fig. 2 Distribution of Cornigerius maeoticus in the native Fig. 3 Distribution of Podonevadne trigona in the native range (open cycles) and sites of first records of its range range (open cycles) and sites of first records of its range expansion (filled cycles). Dashed line indicate the ‘‘north- expansion (filled cycles). Dashed line indicate the ‘‘northern invasion corridor’’ ern invasion corridor’’

123 Hydrobiologia (2007) 590:3–14 7

their maximal abundance in the middle of summer at temperatures above 15°C and typically disap- pearing in months with temperatures below 10°C (Mordukhai-Boltovskoi, 1966; Rivier, 1998; Kry- lov et al., 1999). However, this ‘‘thermophily’’ is relative and may not be the limiting factor for potential species distribution in a latitudinal direction, as all invasive Ponto-Caspian onychopods, like most Cladocera, are able to survive unfavorable cold water conditions in winter as resting eggs in bottom sediments. Most Ponto-Caspian onychopods have a rela- tively high salinity tolerance and can be considered as ‘‘euryhaline’’ species. Cercopagis pengoi, Podonevadne trigona and Cornigerius maeoticus Fig. 4 Distribution of Evadne anonyx in the native range may live in freshwater and in water with a salinity (open cycles) and sites of first records of its range up to 13& (Rivier, 1998). Salinity tolerance of expansion (filled cycles). Dashed line indicate the ‘‘north- Evadne anonyx was considered much narrower, ern invasion corridor’’ from 9 to 13.5& in the native distribution range (Rivier, 1998), but E. anonyx has been recently studies, however, of E. anonyx in recipient and found in the Neva Estuary (easternmost Baltic potential donor areas are needed to validate this Sea) at salinities between 1–3& (Rodionova & hypothesis. Panov, 2006), which indicates the wider salinity tolerance of this species. In contrast with other General patterns of biology of the invasive invasive onychopoda, it is likely that E. anonyx is onychopods unable to survive pure freshwater conditions, which is a potential reason for the absence of an Comprehensive reviews of the biology of the invasion history for this species in reservoirs of Ponto-Caspian onychopods are available else- Ponto-Caspian rivers. where (Mordukhai-Boltovskoi, 1966; Rivier, Analysis of temperature and salinity tolerances 1998). Also, a comprehensive comparative study of these invasive onychopod species, therefore, of C. pengoi variability in body dimensions and indicates that they are potentially able to form population demography in the Caspian, Lake populations in a wide range of inland and coastal Ontario and the Baltic Sea has been recently water ecosystems in temperate regions. published by Grigorovich et al. (2000). In the present paper, we review patterns of biology of Life cycle and reproduction patterns this group, which are essential for understanding the comparatively broad native range of these Like most Cladocera, invasive Ponto-Caspian species, their invasion success in recipient ecosys- onychopods possess an heterogonic reproductive tems and for risk assessment purposes (predic- cycle and are able to undergo parthenogenetic tions of future introductions of invasive species and amphigonic (sexual, or gamogenetic) repro- and their possible ecosystem impacts). Selected duction. As a general feature of most Cladocera, biological traits of Ponto-Caspian invasive ony- onychopods hatch from resting eggs, that survive chopods are given in Table 1. the winter in bottom sediments, in late spring- early summer. For the rest of the summer, they Temperature and salinity tolerance typically reproduce parthenogenetically and then switch to sexual reproduction in the fall to Ponto-Caspian invasive onychopods are usually produce resting ‘‘winter’’ eggs (Rivier, 1998; considered as ‘‘thermophilic’’ species, reaching Rivier, 2004). Mordukhai-Boltovskoi (1966) first

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Table 1 Selected biological traits of invasive Ponto-Caspian onychopods: fe-p = instar III parthenogenetic females, fe-g = instar III gamogenetic females, male = instar III males, numbers in parenthesis indicate range Species Lifestage Length, Height, Fecundity, Temperature Salinity Reference mm mm Eggs ind–1. range, °C range, &

Cercopagis pengoi fe-p 1.73 13 Freshwater—13 Rivier, 1998; Caspian population Grigorovich et al., 2000 Baltic Sea population fe-p 2.41 (2.19–2.53) 5.9 (1–15) 8–24 0.6–3.0 Rodionova & Panov, unpubl. fe-g 2.40 (2.24–2.56) 1.4 (1–2) Male 2.14 (1.85–2.50) Great Lakes population fe-p 1.45 2–13 Freshwater Grigorovich et al., 2000; fe-g 1.58 1–2 Makarevich et al., 2001; Male 1.37 Ojaveer et al., 2001 Volga River population fe-p 1.68–1.83 19.1–23.3 Freshwater Bychek, unpubl. Cornigerius maeoticus fe-p 0.5–0.8 0.6–0.9 Freshwater—13 Rivier, 1998 Ponto-Azov population Male 0.6 0.65 Baltic Sea population fe-p 1.09 7.7 (5–10) 11–21 0.7–1.7 Rodionova & Panov, unpubl. Volga River population fe-p 0.53–0.91 16.2–23.3 Freshwater Bychek, unpubl. Male 0.5 Cornigerius bicornis fe-p 0.6–0.7 Freshwater—13 Rivier, 1998 Ponto-Azov population Evadne anonyx fe-p 2.0–2.1 10–25 9–13.5 Rivier, 1998 Caspian population Male 1.2–1.4 Baltic Sea population fe-p 0.66 1.1 3.9 (1–6) 11–24 1–3 Rodionova & Panov, 2006 fe-g 0.65 1.1 1.7 (1–2) Male 0.49 0.79 yrbooi 20)590:3–14 (2007) Hydrobiologia Podonevadne trigona fe-p 0.4–0.5 11–16 Freshwater—13 Rivier, 1998 Ponto-Azov population Hydrobiologia (2007) 590:3–14 9 noted that gamogenetic reproduction, with the legs (thoracopods I), retain it using their other development of resting ‘‘latent’’ eggs, is often three pairs of thoracic legs (thoracopods II–IV), found in onychopod species that are widely crush the cuticle by using their mandibles and distributed beyond the Caspian—in the Aral Sea suck out the body contents (Rivier, 1998). Exper- and Pontoazov basins, namely in Cercopagis imental studies on the feeding biology of Ponto- pengoi, Cornigerius maeoticus, Evadne anonyx Caspian onychopods are generally lacking (but and Podonevadne trigona. In addition, in the see Witt & Caceres, 2004). Analysis of their gut same species males and winter eggs are more contents and direct observations indicate that numerous in the shallow freezing waters of Azov these species may consume plankton inverte- Sea and lagoons than in the deep Caspian brates, including rotifers, copepods and cladocer- (Mordukhai-Boltovskoi, 1966). ans, and algae (Rivier, 1998). Invading population of C. pengoi in the Neva Field observations of long-term and seasonal Estuary (easternmost Baltic Sea) showed a changes in zooplankton communities invaded by remarkable reproductive strategy, producing a Cercopagis pengoi, showed changes in the abun- large number of resting eggs during the summer dance of some native species, which can be months in 1996 (Panov et al., 1996; Krylov & attributed to the direct predation by C. pengoi. Panov, 1998), followed by a gradual decline in In the Baltic Sea, C. pengoi was found to affect gamogenetic reproduction by 2000. This strategy the population size of the previously abundant is the likely result of selective fish predation on Bosmina coregoni maritima (Ojaveer et al., 2000) more visible sexual females with resting eggs and may potentially affect other groups of zoo- (Panov et al., 2004). Prolonged summer gamoge- plankton (Uitto et al., 1999; Telesh & Ojaveer, netic reproduction was also found in E. anonyx 2002). which has become recently established in the In Lake Ontario, C. pengoi is already playing eastern Gulf of Finland (Rodionova & Panov, an important role in the zooplankton (Ojaveer 2006). et al., 2001; Makarewicz et al., 2001, 2003) and It has been suggested that a large pool of may suppress some native zooplankton species, resting eggs from C. pengoi in the Neva Estuary including rotifers, juvenile copepods and small has enabled this species to achieve rapid popula- cladocerans, namely Bosmina longirostris (Benoit tion growth in recipient ecosystems and to pose et al., 2002; Laxson et al., 2003). an increased risk of dispersal by ships’ ballast water (Panov et al., 1996; Krylov & Panov, 1998; Biotic interactions with other predators Panov et al., 1999). Indeed, this pattern of reproductive strategy has facilitated the secondary Information is scarce on the biotic interactions of invasion of C. pengoi from the eastern Baltic to Ponto-Caspian onychopoda with other predators the North American Great Lakes, which occurred in their native and extended range, but it is just a few years after the establishment of this essential for the estimation of biological resis- species in the eastern Baltic. Populations of tance of already invaded and potential recipient C. pengoi in Lake Ontario in the first years after ecosystems. invasion, also possessed an unusual midsummer In their native range in the Caspian Lake, period of sexual reproduction (Grigorovich et al., onychopods are an important part of the diet of 2000; Makarewicz et al., 2001), which was char- many commercial planktivorous fish (Rivier, acteristic for the source population in the eastern 1998). Recently, the abundance of native zoo- Baltic Sea (Neva Estuary) (Panov et al., 2004). plankton species in the middle and south Caspian has significantly declined, due to the predatory Feeding and predatory impacts impact of the accidentally introduced Atlantic ctenophore Mnemiopsis leidyi (Shiganova et al., Onychopoda are generally considered as active 2001; Shiganova et al., 2004). predators; they capture prey (mainly small plank- In the recipient ecosystems, the Ponto-Caspian tonic crustaceans) with the first pair of thoracic invasive onychopods can also be controlled to

123 10 Hydrobiologia (2007) 590:3–14 some extent by the native and/or introduced goi in this lake. At present, the latter onychopod predators, specifically by fish. In the Baltic Sea, species is the most abundant in Lake Ontario, Cercopagis pengoi is actively consumed by the where B. longimanus is rare compared with all the Baltic herring Clupea harengus membras (Oja- North American Great Lakes. However, the veer et al., 2000; Antsulevich & Va¨lipakka, 2000). biotic interactions of C. pengoi, as well as of Gorokhova et al. (2004) found that gamogenetic other invasive onychopod species, requires fur- females of C. pengoi carrying dark visible resting ther study. eggs are more vulnerable to fish predation (Baltic herring and sprat Sprattus sprattus). These data on the selective predation of zooplanktivorous Qualitative risk assessment fish on gamogenetic females may support our initial hypothesis on the role of invader-selective The first predictions of range expansion of Ponto- fish predation in the rapid evolution of the life Caspian species were produced in one of the early cycle of invading species (Panov et al., 2004). works by Mordukhai-Boltovskoi (1964b). This Results from a study of Lake Ontario fish was the first attempt of ‘‘qualitative’’ risk assess- (alewife Alosa pseudoharengus and rainbow smelt ment for the Ponto-Caspian invasive species, Osmerus mordax), indicate that C. pengoi are based on information relating to their biological effectively consumed by adult alewife. However, patterns, invasion histories and potential path- C. pengoi were not found in the stomachs of ways of introduction. However, Ponto-Caspian juvenile fish, with which this invasive onychopod onychopods were not considered in this paper. species may compete for smaller zooplankton The first qualitative risk assessments for Ponto- (Bushnoe et al., 2003). The latter study also Caspian invasive onychopods were conducted in showed that C. pengoi may reach high abun- the late 1990s, after the invasion of Cercopagis dances in the invaded ecosystem even under pengoi into the Baltic Sea and North American conditions of heavy predation by local fish Great Lakes. Panov et al. (1999) predicted the populations. invasion into the Neva Estuary (eastern Baltic) of Among invertebrate predators, the invasive two common onychopod species, Cornigerius onychopod species Bythotrephes longimanus maeoticus and Podonevadne trigona which had seems to be the most effective predator of the known invasion histories in the Ponto-Caspian Ponto-Caspian C. pengoi both in the Baltic Sea basin via the Volga-Baltic invasion corridor and the North American Great Lakes. At an (European ‘‘northern invasion corridor’’). In- intensively studied location in the Neva Estuary, deed, in 2003 C. maeoticus was first recorded in C. pengoi coexists with native populations of the Neva Estuary (Rodionova et al., 2005), but B. longimanus (source population of B. longim- the second new onychopod invader after C. pengoi anus for North American Great Lakes—see Berg in the Baltic was Evadne anonyx, which was first et al. (2002), with a strong localised negative recorded in the zooplankton of the Neva Estuary relationship between these two predatory cladoc- in 2000 (Rodionova & Panov, 2006). The latter erans. The larger predator, B. longimanus effec- species was not previously considered as a high tively controlling the smaller C. pengoi (Panov risk species, because E. anonyx, before its inva- et al., 2004). The ability of B. longimanus to sion in the eastern Baltic, had no invasion history control C. pengoi in North American Great and was not considered to be able to develop Lakes, has also been recently demonstrated in sustainable populations at salinities below 9& an experimental study of predator-prey relation- (Rivier, 1998). In the eastern Gulf of Finland, ships between these two species by Witt & E. anonyx successfully established itself in areas Caćeres (2004). The high abundance of B. lon- with low water salinities as low as 1–3& (Rodio- gimanus in Lake Erie (Barbiero & Tuchman, nova & Panov, 2006). The unexpected invasion of 2000) may, therefore, be considered a likely E. anonyx into the eastern Baltic Sea may ‘‘ecosystem biotic resistance’’ factor for the indicate that the most common Ponto-Caspian development of abundant populations of C. pen- onychopods (P. trigona, P. camptonyx, P. angusta,

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Polyphemus exiguous, Evadne prolongata) may introduced to the gulf with the ballast water of pose some risk of long-distance intracontinental ships via the northern invasion corridor during transfer if appropriate pathways of introduction 1990–2000. This was a period of signiﬁcant decline are available (shipping along the Volga-Baltic in shipping intensity via the Volga-Baltic inland inland waterway). In general, the Ponto-Caspian waterway caused by an economic crisis and a onychopods pose the highest risk for the Baltic switch to the market economy in Russia. This Sea, as all the alien cladocerans established in the invasion phenomenon can, therefore, attributed eastern Baltic belong to this group (Fig. 5), and to the environmental changes in the recipient the rapid and successful establishment of three ecosystem and its increasing invasibility to the onychopod species has occurred in this region warm water Ponto-Caspian species. during last 15 years. Grigorovich et al. (2003a) also suggested that It is important to note, that during the last two only two invasive Ponto-Caspian onychopods decades invasion rates of Ponto-Caspian species were risk species for the North American Great in the eastern Gulf of Finland (the upper part of Lakes, C. maeoticus and P. trigona. These species the Volga-Baltic waterway) have increased dras- had an invasion history in the Ponto-Caspian tically, with at least 50% of the established Ponto- basin and were initially considered as risk species Caspian species invading the gulf since 1986. In for the eastern Baltic, donor area of invasive addition, during the last 50 years the rates of onychopods Bythotrephes longimanus and Cerco- successfully established alien species in the east- pagis pengoi for the Great Lakes (Panov et al., ern Gulf of Finland were 5-fold higher for Ponto- 1999). Currently only one Ponto-Caspian onycho- Caspian species than for species from other pod species has invaded the Great Lakes (Fig. 5), origins. The most recent Ponto-Caspian invaders but considering the existence of the deﬁned to the Gulf of Finland, onychopod crustaceans invasion corridor between the eastern Baltic C. pengoi, E. anonyx and C. maeoticus, were and the Great Lakes, introduction of other

Fig. 5 Taxonomic composition of alien invertebrate species introduced with ballast water to the Baltic Sea (top) and North American Great Lakes (bottom). Open bars indicate cladocerans, black ﬁlled bars—onychopods. Data used: Grigorovich et al., 2003a, Olenin et al., 2006

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Ponto-Caspian onychopods to North America is Dr. Elizabeth Cook for her careful editing of the possible. C. maeoticus poses the highest risk to manuscript and Dr. Irina Rivier for her valuable discussion and comments. This study has been supported the Great Lakes and E. anonyx is a risk species by the European Commission 6th Framework Programme for the estuaries of the North American east coast Integrated Project ALARM (contract GOCE-CT-2003– (Rodionova & Panov, 2006). 506675), Strategic Targeted Research Project DAISIE It is important to note that the invasion of (contract SSPI-CT-2003–511202), and the Ministry of Education and Science of the Russian Federation C. pengoi to the Laurentian Great Lakes took (contract 02.435.11.4003). place after the implementation of the ballast water management options for ships entering the References Great Lakes, namely the exchange of ballast water in the open ocean, which is currently considered as an effective measure to decrease Antsulevich, A. & P. Va¨lipakka, 2000. Cercopagis pen- the risk of transfer of freshwater organisms by goi—new important food object of the Baltic herring in the Gulf of Finland. International Review of ships. However, as it has been recently shown, Hydrobiology 85: 609–619. that the resting eggs of freshwater invertebrates Avinski, V. A., 1997. Cercopagis pengoi—a new species in may hatch from the ballast water sediments which the Eastern Gulf of Finland ecosystem. Proceedings have previously experienced the influence of salt of the Final Seminar of the Gulf of Finland Year 1996. March 17–18, 1997, Helsinki: 247–256. water (Bailey et al., 2003, 2004, 2005). Thus, Barbiero, R. P. & M. L. Tuchman, 2000. Results from the Ponto-Caspian invasive onychopods producing Great Lakes National Program Office’s biological large numbers of resting eggs, pose a very high open water surveillance Program of the Laurentian risk of introduction with ballast waters, even with Great Lakes for 1998. United States Environmental Protection Agency Report, EPA 905-R-00–006. regular ballast water management procedures Bailey, S. A., I. C. Duggan, C. D. A. van Overdijk, P. T. (specifically in the case of the prolonged seasonal Jenkins & H. J. MacIsaac, 2003. Viability of inverte- gamogenetic reproduction of C. pengoi and, to a brate diapausing eggs collected from residual ballast lesser extent, in E. anonyx in the recipient sediment. Limnology and Oceanography 48: 1701–1710. Bailey, S. A., C. D. A. van Overdijk, I. C. Duggan, T. H. ecosystems), which might be ineffective in the Johengen, D. F. Reid & H. J. MacIsaac, 2004. Salinity case of aquatic invertebrates which produce tolerance of diapausing eggs of freshwater zooplank- resting eggs that accumulate in the sediments of ton. Freshwater Biology 49: 286–295. ballast tanks (MacIsaac et al., 1999; Bailey et al., Bailey, S. A., I. C. Duggan, P. T. Jenkins & H. J. MacIsaac, 2005. Invertebrate resting stages in residual ballast 2005). sediment of transoceanic ships. Canadian Journal of The ability of C. pengoi to effectively colonize Fisheries and Aquatic Sciences 62: 1090–1103. known recipient ecosystems in Europe and North Benoit, H. P., O. E. Johansson, D. M. Warner, W. G. America, despite a severe negative relationship Sprules & L. G. Rudstam, 2002. Assessing the impact of a recent predatory invader: The population with B. longimanus and strong selective fish dynamics, vertical distribution, and potential prey of predation, indicates that ‘‘biological resistance’’ Cercopagis pengoi in Lake Ontario. Limnology and to invasion by Ponto-Caspian onychopods can be Oceanography 47: 626–635. important only on a localised and temporal basis. Berg, D. J., D. W. Garton, H. J. MacIsaac, V. E. Panov & I. V. Telesh, 2002. Changes in genetic structure of Thus, at present these species can be considered North American Bythotrephes populations following as ‘‘high risk’’, in terms of their potential for invasion from Lake Ladoga, Russia. Freshwater range expansion and impact on recipient ecosys- Biology 47: 275–282. _ tems. The application of more accurate quantita- Bielecka, L., M. I. Zmijewska & A. Szymborska, 2000. A new predatory cladoceran Cercopagis (Cercopagis) tive risk assessments for this group requires pengoi (Ostroumov 1891) in the Gulf of Gdan´ sk. further study, including experimental studies of Oceanologia 42: 371–374. salinity tolerance and inoculation rates of the Bij de Vaate, A., K. Jazdzewski, H. A. M. Ketelaars, S. resting stages from ships ballast water and other Gollasch & G. Van der Velde, 2002. Geographical patterns in range extension of Ponto-Caspian macro- human-mediated vectors. invertebrate species in Europe. Canadian Journal of Fisheries and Aquatic Sciences 59: 1159–1174. Acknowledgements We thank the three anonymous Bushnoe, T. M., D. M. Warner, L. G. Rudstam & E. L. reviewers for helpful comments on the paper manuscript, Mills, 2003. Cercopagis pengoi as a new prey item for

123 Hydrobiologia (2007) 590:3–14 13

alewife (Alosa pseudoharengus) and rainbow smelt Jazdzewski, K., 1980. Range extensions of some gam- (Osmerus mordax) in Lake Ontario. Journal of Great maridean species in European inland waters caused Lakes Research 29: 205–212. by human activity. Crustaceana Supplement 6: 85– Charlebois, P. M., M. J. Raffenberg & J. M. Dettmers, 107. 2001. First occurrence of Cercopagis pengoi in Lake Jazdzewski, K. & A. Konopacka, 2002. Invasive Ponto- Michigan. Journal of Great Lakes Research 27: 258– Caspian species in waters of the Vistula and Oder 261. basins and the southern Baltic Sea. In Leppa¨koski E., Cristescu, M. E. A., P. D. N. Hebert, J. D. S. Witt, H. J. S. Gollasch, & S. Olenin (eds), Invasive Aquatic MacIsaac & I. A. Grigorovich, 2001. An invasion Species of Europe. Distribution, Impacts and Man- history for Cercopagis pengoi based on mitochondrial agement. Kluwer Academic Publishers, Dordrecht: gene sequencing. Limnology and Oceanography 46: 384–398. 224–229. Ketelaars, H. A. M., 2004. Range extensions of Ponto- Cristescu, M. E. A. & P. D. N. Hebert, 2002. Phylogeny Caspian aquatic invertebrates in continental Europe. and adaptive radiation in the Onychopoda (Crusta- In H. Dumont et al. (eds), Aquatic Invasions in the cea, Cladocera): evidence from multiple gene se- Black, Caspian and Mediterranean Seas. Kluwer quences. Journal of Evolutionary Biology 15: 838–849. Academic Publishers, The Netherlands: 209–236. Dumont, H. J., 1998. The Caspian Lake: history, biota, Krylov, P. I. & V. E. Panov, 1998. Resting eggs in the life structure, and function. Limnology & Oceanography cycle of Cercopagis pengoi, a recent invader of the 43: 44–52. Baltic Sea. Archiv fu¨ r Hydrobiologie, Advances in Dumont, H. J., 2000. Endemism in the Ponto-Caspian Limnology 52: 383–392. fauna, with special emphasis on the Onychopoda Krylov, P. I., D. E. Bychenkov, V. E. Panov, N. V. (Crustacea). Advances in Ecological Research 31: Rodionova & I. V. Telesh, 1999. Distribution and 181–196. seasonal dynamics of the Ponto-Caspian invader Dumont, H., T. A. Shiganova, & U. Niermann (eds) 2004. Cercopagis pengoi (Crustacea, Cladocera) in the Aquatic Invasions in the Black, Caspian and Medi- Neva Estuary (Gulf of Finland). Hydrobiologia 393: terranean Seas. Kluwer Academic Publishers, The 227–232. Netherlands. Krylov, P. I., P. V. Bolshagin, D. E. Bychenkov, E. N. Galil, B. S., S. Nehring & V. E. Panov, 2007. Waterways as Naumenko, V. E. Panov & Y. Y. Polunina, 2004. invasion highways – Impact of climate change and Invasions of predatory planktonic cladocerans and globalization. In W. Nentwig (ed.), Biological Inva- possible causes of their success. In Alimov A. F. & N. sions. Ecological Studies No. 193, Springer, Berlin. G. Bogutskaya (eds), Biological Invasions in Aquatic 59–74. and Terrestrial Ecosystems. KMK Scientiﬁc Press Gorokhova, E., N. Aladin & H. J. Dumont, 2000. Further Ltd., Moscow: 99–128 (in Russian). expansion of the genus Cercopagis (Crustacea, Bran- Laxson, C. L., K. N. McPhedran, J. C. Makarewicz, I. V. chiopoda, Onychopoda) in the Baltic Sea, with notes Telesh & H. J. MacIsaac, 2003. Effects of the non- on the taxa present and their ecology. Hydrobiologia indigenous cladoceran Cercopagis pengoi on the lower 429: 207–218. food web of Lake Ontario. Freshwater Biology 48: Gorokhova, E., T. Fagerberg & S., Hansson, 2004. Pre- 2094–2106. dation by herring (Clupea harengus) and sprat Leppa¨koski, E., S. Gollasch, P. Gruszka, H. Ojaveer, S. (Sprattus sprattus)onCercopagis pengoi in a western Olenin & V. Panov, 2002. The Baltic—a sea of Baltic Sea bay. ICES Journal of Marine Science 61: invaders. Canadian Journal of Fisheries and Aquatic 959–965. Sciences 59: 1175–1188. Grigorovich, I. A., H. J. MacIsaac, I. K. Rivier, N. V. MacIsaac, H. J., I. A. Grigorovich, J. A. Hoyle, N. D. Yan Aladin & V. E. Panov, 2000. Comparative biology of & V. E. Panov, 1999. Invasion of Lake Ontario by the the predatory cladoceran Cercopagis pengoi from Ponto-Caspian cladoceran predator Cercopagis pen- Lake Ontario, Baltic Sea and Caspian Sea. Archiv fu¨ r goi. Canadian Journal of Fisheries and Aquatic Sci- Hydrobiologie 149: 23–50. ences 56: 1–5. Grigorovich, I. A., H. J. MacIsaac, N. V. Shadrin & E. L. Makarewicz, J. C., I. A. Grigorovich, E. Mills, E. Da- Mills, 2002. Patterns and mechanisms of aquatic maske, M. E. Cristescu, W. Pearsall, M. J. LaVoie, R. invertebrate introductions in the Ponto-Caspian re- Keats, L. Rudstam, P. Hebert, H. Halbritter, T. Kelly, gion. Canadian Journal of Fisheries and Aquatic Sci- C. Matkovich & H. J. MacIsaac, 2001. Distribution, ences 59: 1189–1208. fecundity, and genetics of Cercopagis pengoi (Os- Grigorovich, I. A., R. I. Colautti, E. L. Mills, K. Holeck, A. troumov) (Crustacea, Cladocera) in Lake Ontario. G. Ballert & H. J. MacIsaac, 2003a. Ballast-mediated Journal of Great Lakes Research 27: 19–32. animal introductions in the Laurentian Great Lakes: Makarewicz, J. C., E. Damaske, C. Laxson, H. J. MacIsaac, retrospective and prospective analyses. Canadian & I. A. Grigorovich, 2003. Seasonal and vertical dis- Journal of Fisheries and Aquatic Sciences 60: 740–756. tribution, food web dynamics and contaminant bio- Grigorovich, I. A., T. W. Therriault & H. J. MacIsaac, magniﬁcation of Cercopagis pengoi in Lake Ontario. 2003b. History of aquatic invertebrate invasions in the Proceedings of the 11th Annual Invasive Species Caspian Sea. Biological Invasions 5: 103–115. Conference, 132–141.

123 14 Hydrobiologia (2007) 590:3–14

Mordukhai-Boltovskoi, Ph. D., 1964a. Caspian fauna in Rivier, I. K., 2004. Biology of reproduction in planktonic fresh waters outside the Ponto-Caspian basin. Hyd- crustaceans of the family Cercopagidae (Polyphe- robiologia 23: 159–164. moidae, Cladocera). Zoological Journal 83: 776–787 Mordukhai-Boltovskoi, Ph. D., 1964b. Caspian fauna be- (in Russian). yond the Caspian Sea. Internationale Revue Der Rodionova, N. V., P. I. Krylov & V. E. Panov, 2005. Gesamten Hydrobiologie 49: 139–176. Invasion of the Ponto–Caspian predatory cladoceran Mordukhai-Boltovskoi, Ph. D., 1966. Distribution, biology Cornigerius maeoticus maeoticus (Pengo, 1879) into and morphology of Polyphemidae in fresh and the Baltic Sea. Oceanology 45: 66–68. brackish waters of the Pontocaspian basin. Interna- Rodionova, N. V. & V. E. Panov, 2006. Establishment of tionale Vereinigung fur Theoretische und Ange- the Ponto-Caspian predatory cladoceran Evadne an- wandte Limnologie, Verhandlungen 16: 1677–1683. onyx in the eastern Gulf of Finland, Baltic Sea. Mordukhai-Boltovskoi, Ph. D., 1979. Composition and Aquatic Invasions 1: 7–12. distribution of Caspian fauna in the light of modern Shiganova, T. A., A. M. Kamakin, O. P. Zhukova, V. B. data. Internationale Revue Der Gesamten Hydrobi- Ushivtsev, A. B. Dulimov & E. I. Musaeva, 2001. The ologie 64: 1–38. invader into the Caspian Sea ctenophore Mnemiopsis Ojaveer, H. & A. Lumberg, 1995. On the role of Cerco- and its initial effect on the pelagic ecosystem. pagis (Cercopagis) pengoi (Ostroumov) in Pa¨rnu Bay Oceanology 41: 542–549. and the NE part of the Gulf of Riga ecosystem. Pro- Shiganova, T. A., H. J. Dumont, A. F. Sokolsky, A. M. ceedings of the Estonian Academy of Sciences, Kamakin, D. Tinenkova & E. K. Kurasheva, 2004. Ecology 5: 20–25. Population dynamics of Mnemiopsis leidyi in the Ojaveer, H., A. Lankov, & A. Lumberg, 2000. Conse- Caspian Sea, and effects on the Caspian ecosystem. In quences of invasion of a predatory cladoceran. ICES Dumont H. J., T. A. Shiganova & U. Niermann (eds), C.M. 2000/U:16. Aquatic Invasions in the Black, Caspian, and Medi- Ojaveer, H., A. L. Kuhns, R. P. Barbiero & M. L. Tuch- terranean Seas. Kluwer Academic Publishers, man, 2001. Distribution and population characteristics Dordrecht, Boston, London: 71–111. of Cercopagis pengoi in Lake Ontario. Journal of Teles, I. V. & H. Ojaveer, 2002. The predatory water flea Great Lakes Research 27: 10–18. Cercopagis pengoi in the Baltic Sea: invasion history, Olenin, S, E. Leppa¨koski, & D. Daunys (eds), 2006. Alien distribution and implications to ecosystem dynamics. Species Directory, Baltic Sea Alien Species Database, In Leppa¨koski E., S. Gollasch & S. Olenin (eds), http://www.ku.lt/nemo/alien_species_directory.html . Invasive Aquatic species of Europe—distribution Panov, V. E., P. I. Krylov & I. V. Telesh, 1996. The Cas- impacts and management. Kluwer Academic Pub- pian predatory cladoceran Cercopagis pengoi invades lishers, Dordrecht, Boston, London: 62–65. the Gulf of Finland. BFU Research Bulletin 2: 80–81. Therriault, T. W., I. A. Grigorovich, D. D. Kane, E. M. Panov, V. E., P. I. Krylov & I. V. Telesh, 1999. The St. Haas, D. A. Culver & H. J. MacIsaac, 2002. Range Petersburg harbour profile. In Gollasch, S. & E. expansion of the exotic zooplankter Cercopagis pen- Leppa¨koski (eds), Initial Risk Assessment of Alien goi (Ostroumov) into western Lake Erie and Mus- Species in Nordic Coastal Waters. Nord 1999: 8. kegon Lake. Journal of Great Lakes Research 28: Nordic Council of Ministers, Copenhagen: 225–244. 698–701. Panov, V. E., P. I. Krylov & N. Riccardi, 2004. Role of Uitto, A., E. Gorokhova & P. Va¨lipakka, 1999. Distribu- diapause in dispersal and invasion success by aquatic tion of the non-indigenous Cercopagis pengoi in the invertebrates. Journal of Limnology 63(Suppl. 1): 56– coastal waters of the eastern Gulf of Finland. ICES 69. Journal of Marine Science. 56 Supplement: 49–57. Reid, D. F. & M. I. Orlova, 2002. Geological and evolu- Vanderploeg, H. A., T. F. Nalepa, D. J. Jude, E. L. Mills, tionary underpinnings for the success of Ponto-Cas- K. T. Holeck, J. R. Liebig, I. A. Grigorovich & H. pian species invasions in the Baltic Sea and North Ojaveer, 2002. Dispersal and emerging ecological American Great Lakes. Canadian Journal of Fisheries impacts of Ponto-Caspian species in the Laurentian and Aquatic Sciences 59: 1144–1158. Great Lakes. Canadian Journal of Fisheries and Ricciardi, A. & H. J. MacIsaac, 2000. Recent mass inva- Aquatic Sciences 59: 1209–1228. sion of the North American Lakes by Ponto-Caspian Witt, A. M. & C. E. Caćeres, 2004. Potential predator-prey species. Trends in Ecology & Evolution 15: 62–65. relationships between Bythotrephes longimanus and Rivier, I. K., 1998. The Predatory Cladocera (Onycho- Cercopagis pengoi in southwestern Lake Michigan. poda: Podonidae, Polyphemidae, Cercopagidae and Journal of Great Lakes Research 30: 519–527. Leptodoridae) of the world. Backhuys Publishers, Leiden, The Nertherlands.

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